Increased heat requirement for leaf flushing in temperate woody species over 1980–2012: effects of chilling, precipitation and insolation

Recent studies have revealed large unexplained variation in heat requirement‐based phenology models, resulting in large uncertainty when predicting ecosystem carbon and water balance responses to climate variability. Improving our understanding of the heat requirement for spring phenology is thus urgently needed. In this study, we estimated the species‐specific heat requirement for leaf flushing of 13 temperate woody species using long‐term phenological observations from Europe and North America. The species were defined as early and late flushing species according to the mean date of leaf flushing across all sites. Partial correlation analyses were applied to determine the temporal correlations between heat requirement and chilling accumulation, precipitation and insolation sum during dormancy. We found that the heat requirement for leaf flushing increased by almost 50% over the study period 1980–2012, with an average of 30 heat units per decade. This temporal increase in heat requirement was observed in all species, but was much larger for late than for early flushing species. Consistent with previous studies, we found that the heat requirement negatively correlates with chilling accumulation. Interestingly, after removing the variation induced by chilling accumulation, a predominantly positive partial correlation exists between heat requirement and precipitation sum, and a predominantly negative correlation between heat requirement and insolation sum. This suggests that besides the well‐known effect of chilling, the heat requirement for leaf flushing is also influenced by precipitation and insolation sum during dormancy. However, we hypothesize that the observed precipitation and insolation effects might be artefacts attributable to the inappropriate use of air temperature in the heat requirement quantification. Rather than air temperature, meristem temperature is probably the prominent driver of the leaf flushing process, but these data are not available. Further experimental research is thus needed to verify whether insolation and precipitation sums directly affect the heat requirement for leaf flushing.

[1]  P. Ciais,et al.  Unexpected role of winter precipitation in determining heat requirement for spring vegetation green‐up at northern middle and high latitudes , 2014, Global change biology.

[2]  Annette Menzel,et al.  Recent spring phenology shifts in western Central Europe based on multiscale observations , 2014 .

[3]  Nuno Carvalhais,et al.  Harmonized European Long-Term Climate Data for Assessing the Effect of Changing Temporal Variability on Land–Atmosphere CO2 Fluxes* , 2014 .

[4]  Shilong Piao,et al.  Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species , 2014, Proceedings of the National Academy of Sciences.

[5]  M. Friedl,et al.  A tale of two springs: using recent climate anomalies to characterize the sensitivity of temperate forest phenology to climate change , 2014 .

[6]  J. Dieleman,et al.  Impact of light on leaf initiation: a matter of photosynthate availability in the apical bud? , 2014, Functional plant biology : FPB.

[7]  C. Körner,et al.  Photoperiod and temperature responses of bud swelling and bud burst in four temperate forest tree species. , 2014, Tree physiology.

[8]  Annette Menzel,et al.  Chilling outweighs photoperiod in preventing precocious spring development , 2014, Global change biology.

[9]  Annette Menzel,et al.  Can spatial data substitute temporal data in phenological modelling? A survey using birch flowering. , 2013, Tree physiology.

[10]  A. Mäkelä.  En route to improved phenological models: can space-for-time substitution give guidance? , 2013, Tree physiology.

[11]  I. Janssens,et al.  Sensitivity of leaf unfolding to experimental warming in three temperate tree species , 2013 .

[12]  P. Ciais,et al.  Asymmetric effects of daytime and night-time warming on Northern Hemisphere vegetation , 2013, Nature.

[13]  Yann Vitasse,et al.  Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. , 2013, The New phytologist.

[14]  O. Sonnentag,et al.  Climate change, phenology, and phenological control of vegetation feedbacks to the climate system , 2013 .

[15]  Mark D. Schwartz,et al.  Phenology: An Integrative Environmental Science , 2013, Springer Netherlands.

[16]  Christian Körner,et al.  Photoperiod sensitivity of bud burst in 14 temperate forest tree species , 2012 .

[17]  Ivan A. Janssens,et al.  The Impact of Winter and Spring Temperatures on Temperate Tree Budburst Dates: Results from an Experimental Climate Manipulation , 2012, PloS one.

[18]  Eike Luedeling,et al.  Climate change impacts on winter chill for temperate fruit and nut production: A review , 2012 .

[19]  Mirco Migliavacca,et al.  On the uncertainty of phenological responses to climate change, and implications for a terrestrial biosphere model , 2012 .

[20]  Ke Zhang,et al.  Satellite detection of increasing Northern Hemisphere non-frozen seasons from 1979 to 2008: Implications for regional vegetation growth , 2012 .

[21]  Philippe Ciais,et al.  Terrestrial biosphere model performance for inter‐annual variability of land‐atmosphere CO2 exchange , 2012 .

[22]  Ivan A. Janssens,et al.  Bayesian comparison of six different temperature-based budburst models for four temperate tree species , 2012 .

[23]  S. Malyshev,et al.  Uncertainties in terrestrial carbon budgets related to spring phenology , 2012 .

[24]  Y. Xue,et al.  Terrestrial biosphere models need better representation of vegetation phenology: results from the North American Carbon Program Site Synthesis , 2012 .

[25]  David Basler,et al.  What role for photoperiod in the bud burst phenology of European beech , 2012, European Journal of Forest Research.

[26]  Yanhong Tang,et al.  Altitude and temperature dependence of change in the spring vegetation green-up date from 1982 to 2006 in the Qinghai-Xizang Plateau , 2011 .

[27]  A. Donnelly,et al.  The ecological significance of phenology in four different tree species: effects of light and temperature on bud burst , 2011, International journal of biometeorology.

[28]  Sylvain Delzon,et al.  Assessing the effects of climate change on the phenology of European temperate trees , 2011 .

[29]  Miaogen Shen,et al.  Spring phenology was not consistently related to winter warming on the Tibetan Plateau , 2011, Proceedings of the National Academy of Sciences.

[30]  D. Kohda,et al.  Dual role of the receptor Tom20 in specificity and efficiency of protein import into mitochondria , 2010, Proceedings of the National Academy of Sciences.

[31]  F. Woodward,et al.  Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate , 2010, Science.

[32]  I. Janssens,et al.  Climatic characteristics of heat waves and their simulation in plant experiments , 2010 .

[33]  R. Borchert,et al.  Seasonal variation in daily insolation induces synchronous bud break and flowering in the tropics , 2010, Trees.

[34]  Jacques Roy,et al.  Changes in leaf phenology of three European oak species in response to experimental climate change. , 2010, The New phytologist.

[35]  Christian Körner,et al.  Phenology Under Global Warming , 2010, Science.

[36]  Constance A. Harrington,et al.  Modeling the effects of winter environment on dormancy release of Douglas-fir , 2010 .

[37]  Peter E. Thornton,et al.  Systematic assessment of terrestrial biogeochemistry in coupled climate–carbon models , 2009 .

[38]  Sylvain Delzon,et al.  Leaf phenology sensitivity to temperature in European trees: do within-species populations exhibit similar responses? , 2009 .

[39]  U. Chung,et al.  Using urban effect corrected temperature data and a tree phenology model to project geographical shift of cherry flowering date in South Korea , 2009 .

[40]  Tapio Linkosalo,et al.  A comparison of phenological models of leaf bud burst and flowering of boreal trees using independent observations. , 2008, Tree physiology.

[41]  P. Ciais,et al.  Net carbon dioxide losses of northern ecosystems in response to autumn warming , 2008, Nature.

[42]  Heinz Wanner,et al.  Grape harvest dates as a proxy for Swiss April to August temperature reconstructions back to AD 1480 , 2007 .

[43]  Philippe Ciais,et al.  Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades , 2007 .

[44]  Yiqi Luo,et al.  Divergence of reproductive phenology under climate warming , 2007, Proceedings of the National Academy of Sciences.

[45]  Heikki Hänninen,et al.  A framework for modelling the annual cycle of trees in boreal and temperate regions , 2007 .

[46]  Yuhui Wang,et al.  Simulating phenological characteristics of two dominant grass species in a semi-arid steppe ecosystem , 2007, Ecological Research.

[47]  Rik Leemans,et al.  Faculty Opinions recommendation of European phenological response to climate change matches the warming pattern. , 2006 .

[48]  Dennis D. Baldocchi,et al.  A multiyear evaluation of a Dynamic Global Vegetation Model at three AmeriFlux forest sites: Vegetation structure, phenology, soil temperature, and CO2 and H2O vapor exchange , 2006 .

[49]  Gordon B. Bonan,et al.  Simulating Springtime Temperature Patterns in the Community Atmosphere Model Coupled to the Community Land Model Using Prognostic Leaf Area , 2004 .

[50]  A. Strahler,et al.  Climate controls on vegetation phenological patterns in northern mid‐ and high latitudes inferred from MODIS data , 2004 .

[51]  John Harte,et al.  INTEGRATING EXPERIMENTAL AND GRADIENT METHODS IN ECOLOGICAL CLIMATE CHANGE RESEARCH , 2004 .

[52]  V. Dose,et al.  Bayesian analysis of climate change impacts in phenology , 2004 .

[53]  J. Grace,et al.  Climate and the meristem temperatures of plant communities near the tree-line , 1989, Oecologia.

[54]  K. Price,et al.  Response of seasonal vegetation development to climatic variations in eastern central Asia , 2003 .

[55]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[56]  A. Fitter,et al.  Rapid Changes in Flowering Time in British Plants , 2002, Science.

[57]  T. Rötzer,et al.  Response of tree phenology to climate change across Europe , 2001 .

[58]  J. Partanen,et al.  Effect of accumulated duration of the light period on bud burst in Norway spruce (Picea abies) of varying ages , 2001 .

[59]  I. Chuine,et al.  A unified model for budburst of trees. , 2000, Journal of theoretical biology.

[60]  Pierre Friedlingstein,et al.  A global prognostic scheme of leaf onset using satellite data , 2000 .

[61]  Heikki Hänninen,et al.  Effects of photoperiod and temperature on the timing of bud burst in Norway spruce (Picea abies). , 1998, Tree physiology.

[62]  Denis-Didier Rousseau,et al.  Fitting models predicting dates of flowering of temperate‐zone trees using simulated annealing , 1998 .

[63]  R. Calamassi,et al.  Geographic variation and bud dormancy in beech seedlings (Fagus sylvatica L) , 1996 .

[64]  K. Kramer.  A modelling analysis of the effects of climatic warming on the probability of spring frost damage to tree species in the Netherlands and Germany , 1994 .

[65]  Koen Kramer,et al.  Selecting a model to predict the onset of growth of Fagus sylvatica , 1994 .

[66]  D. W. Stewart,et al.  Appearance time, expansion rate and expansion duration for leaves of field-grown maize (Zea mays L.) , 1994 .

[67]  O. M. Heide,et al.  Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. , 1993, Physiologia plantarum.

[68]  Heikki Hänninen,et al.  Modelling bud dormancy release in trees from cool and temperate regions. , 1990 .

[69]  E. Kandel,et al.  Proceedings of the National Academy of Sciences of the United States of America. Annual subject and author indexes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[70]  M. Cannell,et al.  Date of budburst of fifteen tree species in Britain following climatic warming , 1989 .

[71]  Gregory A. Lang,et al.  Endo-, Para-, and Ecodormancy: Physiological Terminology and Classification for Dormancy Research , 1987, HortScience.

[72]  R. Darnell,et al.  Endodormancy, paradormancy, and ecodormancy—physiological terminology and classification for dormancy research , 1987 .

[73]  M. Cannell,et al.  Thermal time, chill days and prediction of budburst in Picea sitchensis , 1983 .

[74]  Lloyd T. Wilson,et al.  Degree-days: An aid in crop and pest management , 1983 .

[75]  Risto Sarvas,et al.  Investigations on the annual cycle of development of forest trees. Active period. , 1972 .

[76]  T. Perry.  Dormancy of Trees in Winter , 1971, Science.

[77]  G. Baskerville,et al.  Rapid Estimation of Heat Accumulation from Maximum and Minimum Temperatures , 1969 .

[78]  Harry Smith,et al.  THE CHEMICAL REGULATION OF THE DORMANCY PHASES OF BUD DEVELOPMENT , 1964 .

[79]  Jen-Yu Wang,et al.  A Critique of the Heat Unit Approach to Plant Response Studies , 1960 .

[80]  P. Wareing.  Growth Studies in Woody Species V. Photoperiodism in Dormant Buds of Fagus sylvatica L. , 1953 .

[81]  F. Coville.  THE INFLUENCE OF COLD IN STIMULATING THE GROWTH OF PLANTS , 1920 .